Article Adult Postabdomen, Immature Stages and Biology of Euryommatus mariae Roger, 1856 (Coleoptera: : ), a Legendary in Europe

Rafał Gosik 1,*, Marek Wanat 2 and Marek Bidas 3

1 Department of Zoology and Nature Protection, Institute of Biological Sciences, Maria Curie–Skłodowska University, Akademicka 19, 20-033 Lublin, Poland 2 Museum of Natural History, University of Wrocław, Sienkiewicza 21, 50-335 Wrocław, Poland; [email protected] 3 ul. Prosta 290 D/2, 25-385 Kielce, Poland; [email protected] * Correspondence: [email protected]

Simple Summary: Euryommatus mariae is a legendary weevil in Europe, first described in the 19th century and not collected through the 20th century. Though rediscovered in the 21st century at few localities in Poland, Austria, and Germany, it remains one of the rarest of European , and its biology is unknown. We present the first descriptions of the and pupa of E. mariae, and confirm its saproxylic lifestyle. The differences and similarities between immatures of E. mariae and the genera Coryssomerus, and Eulechriopus are discussed, and a list of larval characters common to all Conoderitae is given. The characters of adult postabdomen are described and illustrated for the first time for diagnostic purposes. Our study confirmed the unusual   structure of the male endophallus, equipped with an extremely long ejaculatory duct enclosed in a peculiar fibrous conduit, not seen in other weevils. We hypothesize that the extraordinarily long Citation: Gosik, R.; Wanat, M.; Bidas, and spiral spermathecal duct is the female’s evolutionary response to the male’s extremely long M. Adult Postabdomen, Immature intromittent organ. Stages and Biology of Euryommatus mariae Roger, 1856 (Coleoptera: Abstract: The larva and pupa of the saproxylic Euryommatus mariae Roger, 1857, the weevil species Curculionidae: Conoderinae), a extremely rare in Europe, are described from Poland. It was reared from galleries in dead branches Legendary Weevil in Europe. Insects of a fallen spruce Picea abies. The larval morphology is compared with available larval descriptions of 2021, 12, 151. https://doi.org/ 10.3390/insects12020151 other genera of the supertribe Conoderitae, namely, the Palaearctic Coryssomerus, and the Nearctic Cylindrocopturus and Eulechriopus. The specific characters of the male and female postabdomen are

Academic Editor: Paulo A. V. Borges described and illustrated, expressing the peculiar structure of endophallus and spermathecal duct, Received: 22 December 2020 not seen in any other weevil species. A hypothesis regarding the mechanics of mating in this species Accepted: 7 February 2021 is proposed. Euryommatus mariae is recorded for the first time to occur in China. Published: 11 February 2021 Keywords: ; weevils; Curculionoidea; Conoderitae; Coryssomerini; genital structures; larva; Publisher’s Note: MDPI stays neutral pupa; saproxylic species; spruce with regard to jurisdictional claims in published maps and institutional affil- iations. 1. Introduction The Conoderinae, Schoenherr, 1833, formerly long known under the com- monly accepted junior name Zygopinae Lacordaire, 1866, has been quite recently applied, Copyright: © 2021 by the authors. as the oldest available name, to a much larger group of weevils, including the former sub- Licensee MDPI, Basel, Switzerland. families , , and Orobitidinae, and nowadays comprises over 7500 This article is an open access article described species in 940 genera. The former four were reduced in rank to su- distributed under the terms and pertribes, among which Conoderitae is the second largest, with approximately 2200 species conditions of the Creative Commons in 212 genera worldwide [1]. However, Conoderitae seems to be the least known taxonomi- Attribution (CC BY) license (https:// cally among the four conoderine supertribes, and the real number of extant species must be creativecommons.org/licenses/by/ several times higher. They are abundant and diverse in samples from rain forest canopies. 4.0/).

Insects 2021, 12, 151. https://doi.org/10.3390/insects12020151 https://www.mdpi.com/journal/insects Insects 2021, 12, 151 2 of 22

For example, at least 520 species were counted during an inventory at La Selva Biological Station in Costa Rica by H. Hespenheide [2], the number updated to 559 species until 2009 (H. Hespenheide, personal communication). While common and hyperdiverse in tropical and subtropical zones, the group is highly under-represented in the Western Palaearctic, in fact by just a single —Coryssomerini— with two genera and four species [3,4]. The strictly Western Palaearctic Coryssomerus consists of C. capucinus (Beck, 1817), widespread in Europe and the Caucasus, along with two much less well-known North African species. In the second genus, Euryommatus Roger, only its type species E. mariae Roger, 1857 was originally described from Europe, while eight further species currently attributed to Euryommatus live in Eastern Asia, Asia Minor or the Arabian Peninsula [3,4]. The only European species E. mariae ultimately turned out to be a Euro-Siberian element, relictual in Europe, but widely distributed throughout Siberia to the Russian Far East, eastern China (the first record here), the Korean Peninsula, and Japan [3–7]. In Europe, Euryommatus mariae has always been a mysterious and indeed legendary weevil. Described by Roger [8] from a locality at Rudy near Ku´zniaRaciborska (Upper Silesia—the type locality, now in Poland), it was not found again in Silesia or anywhere else in the whole of Poland for over a century. Subsequent records from Europe have been very scarce: All come from the 19th century and only from Austria (Salzburg vic.) [9], and Latvia [10]. The occurrence of E. mariae in Poland was finally confirmed after 140 years by Stachowiak [11], who collected a single specimen in the Białowieza˙ Primeval Forest (NE Poland). In the 21st century, the species has been found at several new localities in central Europe. In Poland, further specimens were collected in the Swi˛etokrzyskieMts´ in central Poland, near the village of Cisów [12]. Recently, the weevil was recorded in southern Bavaria in Germany [13]. At the same time, it was rediscovered in Austria, in the East Tyrol exclave [14]. Euryommatus mariae was also recorded in Slovenia, European part of Russia, and Cyprus in recent Palaearctic catalogs [3,4], but these country records are not supported with literature data. Moreover, the latter record is apparently a misidentification, since just an unidentified species of Euryommatus is listed from Cyprus in the recent catalog of Curculionoidea of this island [15]. The occurrence of E. mariae on this Mediterranean island seems rather unlikely. Unlike Coryssomerus capucinus, which develops on several herbaceous species of the Asteraceae, little is known about the host associations of Euryommatus mariae and its congeners. In Austria, it was beaten from ‘Pinus alba’ by Sartorius [9], and probably on this basis, Gerhardt [16,17] presumed its association with fir Abies alba Mill. In Siberia, it develops in dying branches of Abies sibirica Ledb. [18], but the adults were also collected from Pinus sylvestris L. (Legalov, personal communication). In Germany, the weevil was also collected from pine branches, albeit of Pinus mugo subsp. uncinata (DC.) Domin. In turn, all 28 Polish specimens of E. mariae, collected in the forest near Cisów, were obtained using spiral screen-trunk traps (‘Geolas’ trap) deployed on the trunks of spruce Picea abies (L.) H. Karst. This may indicate an oligophagous type of host association within the Pinaceae. Being familiar with the former sampling area in Cisów, we undertook an investigation there to find immature stages of Euryommatus mariae in branches from a dead and fallen spruce Picea abies. Laboratory examination of these branches in March 2012 revealed a pupa, found by M. Bidas, who reared it to the adult. The site was revisited in the same month to obtain further material. Here, we give the first morphological description of the larva and pupa of E. mariae obtained from the above-mentioned spruce branches. The larval characters of Euryommatus are compared with available descriptions of some Nearctic species of Conoderitae, including the conifer-associated Cylindrocopturus furnissi Buchanan.

2. Materials and Methods The immature specimens used in this study: A premature (probably fourth) instar larva (one ex.), a mature larva (2 exx.), and pupae ( )(2 exx). All were collected from ♀ Insects 2021, 12, 151 3 of 22

one site: Cisów, forest district Daleszyce, forest comp. 144, 50.74N/20.86E, 264 m alt., 22.03.2012, branches cut from a fallen spruce trunk, leg. M. Wanat and M. Bidas. The larvae and pupae are deposited in the collections of the Department of Zoology and Nature Protection, Maria Curie-Skłodowska University (Lublin, Poland). The ten adult specimens examined are all from the collection of M. Wanat, stored at the Museum of Natural History, University of Wrocław: Poland: Swi˛etokrzyskieMts:´ Cisów, o. 144, UTM: DB82, 7–BMw G.Sw. 2, 29–31 VIII 2006, screen traps on spruce, 2 3 , leg. J. Borowski; same locality, reared ex dead spruce branches, imagines emerged 6 II♂ 2008♀ (1 ex.), 17 I 2012 (1 ex.), 1 III 2012, 1 , leg. M. Bidas. China (East): Harbin, 1 . Russia: W Siberia: Altai, Teletzkoe Lake, 12 VII♂ 1975, 1 1 , leg. F. I. Opanassenko. ♀ ♂ ♀ 2.1. Habitat The locality near Cisów is a part of large, forested areas within boundaries of the Cisowsko-Orłowi´nskiLandscape Park, undergoing sustainable forest management. It is a natural mixed humid coniferous forest, with dominant pine and spruce, and a small admixture of deciduous trees, mainly birch, alder, and oak (Figure1A). The forest floor is mossy, and the undergrowth consists primarily of spruce saplings. The site is situated very close to the open peat bog area of the Białe Ługi Reserve. The fallen spruce sampled for Euryommatus immatures was a dead tree of medium age, with its side branches still largely covered with loose bark (Figure1B); hence, it must have lain there for months rather than years, being nearly or quite dead when it fell. Several branches about 3–4 cm in diameter were sawn into pieces and taken to the laboratory in Wrocław. The branches were examined by carefully removing fragments of bark, under which a number of short and simple galleries could be seen. Four galleries contained single larvae, and in one, a pupa of Euryommatus was detected in a terminal elongate-oval and only slightly deepened pupal chamber (Figure1C). The largest larva was left alive in its gallery, where it pupated

Insects 2021, 12, x FOR PEER REVIEW 4 of 24 a few days later. All the immature stages were preserved for morphological studies.

Figure 1. Biotope of Euryommatus mariae. (A) Forest in Cisów (Świętokrzyskie Mts., Poland); (B) deadFigure spruce hosting 1. theBiotope larvae; (C) larval ofgallery.Euryommatus mariae.(A) Forest in Cisów (Swi˛etokrzyskieMts.,´ Poland); (B)

dead spruce hosting the larvae; (C) larval gallery. Insects 2021, 12, 151 4 of 22

2.2. Methods 2.2.1. Morphological Studies—Immature Specimens All the specimens described were fixed in 95% ethanol and examined under an optical stereomicroscope (Olympus SZ 60 and SZ11) with calibrated oculars. The graduation was scaled up to 1/10 mm. Measurements were made under a 30× magnification. The following measurements of larval instars were made: Body length (BL), body width (BW) (at the third abdominal segment), and width of the head capsule (HW). The pupal measurements included body length (BL), body width (BW) (at the level of the mid legs), head width (HW) (at the level of the eyes), length of rostrum (RL), and width of pronotum (PW). The drawings and outlines were made using a drawing tube (MNR–1) installed on a stereomicroscope (Amplival Pol-d, Carl Zeiss Jena, Germany). and processed by computer software (Corel Photo-Paint X7, Corel Draw X7 (Corel Inc. Austin, TX, USA). Slide preparation basically follows May [19]. The larvae selected for study under the microscope were cleared in 10% potassium hydroxide (KOH), then rinsed in distilled water and dissected. After clearing, the head, mouthparts, and body (thoracic and abdominal segments) were separated and mounted on permanent microscope slides in Faure–Berlese fluid (50 g gum arabic and 45 g chloral hydrate dissolved in 80 g of dissolved water and 60 cm3 of glycerol) [20]. The photographs were taken using an Olympus BX63 microscope and processed with Olympus cellSens Dimension software. The larvae selected for SEM imaging (scanning electron microscope) were first dried in absolute ethanol (99.8%), then rinsed in acetone, treated by CPD (Critical Point Drying), and finally gold-plated. TESCAN Vega 3 SEM was used to examine selected structures. The general terminology and chaetotaxy follow Ander- son [21], May [19], Marvaldi [22–25], and Skuhrovec et al. [26]; the antennae terminology follows Zacharuk [27].

2.2.2. Morphological Abbreviations Abd. I–X—abdominal segments 1–10, Th. I–III—thoracic segments 1–3, at—antenna, clss—clypeal sensorium, ds—digitiform sensillum, st—stemmata, Se—sensorium, sa— sensillum ampullaceum, sb—sensillum basiconicum, snp—sensillae pore, ss—sensillum styloconicae, tra—terminal receptive area, lr—labral rods, ur—urogomphus; setae: als— anterolateral, ams—anteromedial, as—alar (larva), as—apical (pupa), cls—clypeal, d— dorsal (pupal abdomen), des—dorsal (larval head), dms—dorsal malar, ds—discal (pupal prothorax), ds—dorsal (larval abdomen), eps—epipleural, es—epistomal, eus—eusternal, fs—frontal, les—lateral epicranial, ligs—ligular, lrs—labral, ls—lateral, lsts—laterosternal, mbs—malar basiventral, mds—mandibular, mes—median, mps—maxillary palp, pda— pedal, pds—postdorsal, pls—posterolateral, pes—postepicranial, pfs—palpiferal, pms— postlabial, prms—prelabial, prns—pronotal, prs—prodorsal, ps—pleural, sls—super lateral, sos—superorbital, ss—spiracular, stps—stipal, sts—sternal, ves—ventral, vms—ventral malar, vs—vertical. HW—head width, BL—body length, BW—body width, RL—rostrum length, PW—pronotum width.

2.2.3. Morphological Studies—Adult Specimens Images of adult specimens were taken with a Leica M205C stereomicroscope and attached digital camera JVC KYF75. The images obtained were combined using the Au- toMontage software of Syncroscopy (Cambridge, UK), and enhanced using Adobe Photo- shop CS2 program. The aedeagus was photographed under transmitted light using the same equipment, while the details of the conduit of the ejaculatory duct were illustrated using a Nikon Eclipse Ni compound microscope with attached Nikon D7500 camera, and the stacks were combined using the Helicon Focus software (ver. 7.5.1 Pro, Helicon Soft Ltd., Kharkiv, Ukraine). Genitalia preparations were made according to the standard method after a maceration of the separated abdomen for 5–10 min in hot KOH solution. Membranous structures were stained in a glycerol solution of chlorazol black. After rinsing in distilled water, further Insects 2021, 12, x FOR PEER REVIEW 6 of 24

were stained in a glycerol solution of chlorazol black. After rinsing in distilled water, fur- ther separation and examination of the terminal segments and genitalia were carried out Insects 2021, 12, 151 5 of 22 in pure glycerol on a microscope slide, under both stereoscopic and compound micro- scopes. Only the spermatheca was first photographed in distilled water, to illustrate its natural shape, before the eventual collapse of its wall after transfer to glycerol. After the separationstudy, all andthe examinationparts were stored of the terminalin glycerol segments in a microvial and genitalia pinned were beneath carried outthe inspecimen, purewhile glycerol the abdominal on a microscope ventrites slide, were under glued both onto stereoscopic a card adjacent and compound to the microscopes.specimen. Only the spermatheca was first photographed in distilled water, to illustrate its natural shape, before the eventual collapse of its wall after transfer to glycerol. After the study, all the3. Results parts were stored in glycerol in a microvial pinned beneath the specimen, while the abdominal3.1. Description ventrites of the were Larva glued of ontoEuryommatus a card adjacent Mariae to the specimen.

3. ResultsPremature larva (4th instar): HW: 0.70 mm (rest of the body deformed). 3.1. DescriptionMature larva of the Larva(5th instar): of Euryommatus HW: 0.95 Mariae mm; 0.95 mm; BL: 3.35 mm; 3.50 mm; BW: 1.60 mm; 1.40 mm. Premature larva (4th instar): HW: 0.70 mm (rest of the body deformed). MatureGeneral larva habitus (5th instar):(Figure HW: 2). Living 0.95 mm; larva 0.95 is mm; pure BL: white, 3.35 mm; with 3.50 a pale mm; BW:brown 1.60 head mm; capsule. 1.40Its b mm.ody is rather stout, curved, and rounded in the cross section. The prothorax small, withGeneral a slightly habitus pigmented(Figure2). pronotal Living larva shield; is pure meso white,- and with metathorax a pale brown almost head equal capsule. in size. The Itsmeso body- and is rather metathorax stout, curved, are each and roundeddivided in dorsally the cross into section. two lobesThe prothorax (prodorsal small, lobes very withsmall, a slightlypostdorsal pigmented lobes prominent). pronotal shield; The meso-pedal andlobes metathorax of thoracic almost segments equal are in size.isolated and Theconical. meso- Abdominal and metathorax segments are each I and divided II are dorsally of similar, into twomedium lobes (prodorsalsize, and segments lobes very III–V are small,the biggest postdorsal. The lobes next prominent). segments Thetaper pedal towards lobes ofposterior thoracic body segments end. are Abdominal isolated and segments conical. Abdominal segments I and II are of similar, medium size, and segments III–V are I–VII are narrow, and the prodorsal lobe, and always well-developed postdorsal lobe is the biggest. The next segments taper towards posterior body end. Abdominal segments I–VIIdivided are narrow,into three and parts the prodorsal (first and lobe, third and wide, always second well-developed narrow). Segment postdorsal VIII lobe, with is narrow dividedprodorsal into lobe three and parts wide (first postdorsal and third wide, lobe second, is divided narrow). into Segment two folds VIII, equal with narrow in length. The prodorsalepipleural lobe lobes and of wide segments postdorsal I–VI lobe,are slightly is divided conical, into two and folds prominent equal in on length. segments The VII and epipleuralVIII. The l lobesaterosternal of segments and I–VIeusternal are slightly lobes conical,of segments and prominent I–VIII are onconical segments and VIIweakly iso- andlated. VIII. Abdominal The laterosternal segment and IX eusternal is undivided lobes ofdorsally. segments Abdominal I–VIII are conical segment and X weakly is divided into isolated.four lobes Abdominal of almost segment equal size. IX is The undivided anus is dorsally. situated Abdominal terminally. segment Only the X is pronotal divided sclerites intoare fourbrownish, lobes of and almost the remaining equal size. Thethoracic anus and is situated all abdominal terminally. segments Only the are pronotal white or grey- sclerites are brownish, and the remaining thoracic and all abdominal segments are white ish. The body cuticle is densely covered with asperities, taking a form of thorns (Figure or greyish. The body cuticle is densely covered with asperities, taking a form of thorns (Figure3A–D),3A–D), and on and dorsal on dorsal parts parts of abdominal of abdominal segments segments,, additionally additionally,, with with peculiar peculiar elongate elongateplate-like plate-like asperities asperities—each—each parallel parallel to long to long body body axis axis and and bicornuate, bicornuate, arranged arranged in in trans- transverseverse rows rows (Figure (Figure 3C).3C). AllAll spiraclesspiracles are are bicameral; bicameral; thoracic thoracic (Figure (Figure4A) placed 4A) latero- placed latero- ventrallyventrally are are on on the the prothorax; prothorax; abdominal abdominal spiracles spiracles (Figure (Figure4B) are 4B) placed are medio-laterally placed medio-laterally onon segments segments I–VIII. I–VIII.

FigureFigure 2. 2. EuryommatusEuryommatus mariae mariaelive live larva larva photographed photographed in in a gallerya gallery under under a Leica a Leica stereoscopic stereoscopic mi- microscope,croscope, length length 3.8 mm.mm.

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Figure 3. 3. EuryommatusEuryommatus mariae mariae maturemature larva, larva, habitus habitus,, and and cuticle cuticle (SEM (SEM micrographs micrographs,, TESCAN TESCAN OR- ORSAY SAYFigureHOLDIND, HOLDIND, 3. Euryommatus Brno, Brno, Czech Czech mariae Republic). Republic mature). (larva,A (A)) Lateral L ateralhabitus viewview, and of cuticle head and and (SEM thorax; thorax; micrographs (B ()B v)entral ventral, TESCAN view view of ofOR- the SAY HOLDIND, Brno, Czech Republic). (A) Lateral view of head and thorax; (B) ventral view of theabdominal abdominal segment segment I; ( CI; )(C dorsal) dorsal view view of of the the abdominal abdominal segment segment I; I; ( D(D)) lateral lateral viewview ofof thethe abdominalab- dominalthe abdominal segment segment I (setae: I; as (—C)alar, dorsal ps— viewpleural, of the eps —abdominalepipleural, segment eus—eusternal, I; (D) lateral pda— pedal,view of pds the— ab- segment I (setae: as—alar, ps—pleural, eps—epipleural, eus—eusternal, pda—pedal, pds—postdorsal, postdorsal,dominal segment prns—pronotal, I (setae: asprs——alar,prodorsal, ps—pleural, ss—spiracular). eps—epipleural, eus—eusternal, pda—pedal, pds— postdorsal,prns—pronotal, prns—prspronotal,—prodorsal, prs—ssprodorsal,—spiracular). ss—spiracular).

Figure 4. Euryommatus mariae mature larva, spiracles. (A) Spiracle of prothorax; (B) spiracle of ab- dominal segment I. Figure 4. Euryommatus mariae mariae maturemature larva, larva, spiracles. spiracles. (A (A) )S Spiraclepiracle of of prothorax; prothorax; (B (B) s)piracle spiracle of of ab- ab- dominal segment I.

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Chaetotaxy (the number of setae is given for one side of the body) (Figure5A–C). SetaeChaetotaxy of various (the lengths, number fromof setae very is given long fo tor one minute, side of always the body) in the (Figure form 5A of– hairs.C). Setae Thorax of(Figure various5A): length Prothoraxs, from very with long eight to longminute, and always two medium in the formprns of(eight hairs. onThorax pronotal (Figure sclerite, 5A):next Prothorax two above with the eight spiracle), long and two two long mediumps, and prns two (eight medium on pronotaleus. Meso- sclerite, and next metathorax two aboveeach withthe spiracle) one medium, two longprs and ps, and four twopds mediumof various eus length. Meso (first- and long, metathorax second each medium, with third, oneand medium fourth long),prs and alar four area pds with of various one medium length as(first, three long,ss ofsecond various medium, length third (two, and long and fourthone min), long), one alar long areaeps with, one one long mediumps, and as one, three medium ss of variouseus. Pedal length areas (two of long thoracic and segmentsone mineach), one with long six variablyeps, one long sized pspda, and. Abdomen one medium (Figure eus. 5PedalB,C): Segmentsareas of thoracic I–VII withsegments one short eachprs, with five pdssix variably(first, third, sized and pda. fifthAbdomen medium, (Figure second, 5B,C): and Segments fourth I short–VII with to minute), one short two ss prs(first, five minute, pds (first, second third medium),, and fifth twomedium,eps (one second medium, and fourth and one short min), to twominute),ps (one two medium ss (first minute, second medium), two eps (one medium and one min), two ps (one medium and one min), one medium lsts and two medium eus. Abdominal segment VIII with one and one min), one medium lsts and two medium eus. Abdominal segment VIII with one short prs, three very long pds, and one long ss (chaetotaxy of next folds as on segment VII). short prs, three very long pds, and one long ss (chaetotaxy of next folds as on segment VII). Abdominal segment IX with three very long ds, three ps (one long, one medium, and one Abdominal segment IX with three very long ds, three ps (one long, one medium, and one min), and two medium sts. Abdominal segment X with three ts (two short and one minute) min), and two medium sts. Abdominal segment X with three ts (two short and one minute) on each lobe. on each lobe.

FigureFigure 5. 5.EuryommatusEuryommatus mariae mariae maturemature larva, larva, habitus habitus,, and chaetotaxy. and chaetotaxy. (A) Dorsal (A) view; Dorsal (B view;) lateral (B ) lateral view; (C) ventral view (Th. I–III—thoracic segments 1–3, Abd. I–X—abdominal segments 1–10, view; (C) ventral view (Th. I–III—thoracic segments 1–3, Abd. I–X—abdominal segments 1–10, setae: as—alar, ps—pleural, eps—epipleural, ds—dorsal, lsts—laterosternal, eus—eusternal, pda—pedal, pds—postdorsal, prns—pronotal, prs—prodorsal, ss—spiracular, sts—sternal, ts—terminal).

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setae: as—alar, ps—pleural, eps—epipleural, ds—dorsal, lsts—laterosternal, eus—eusternal, pda— pedal, pds—postdorsal, prns—pronotal, prs—prodorsal, ss—spiracular, sts—sternal, ts—terminal).

Insects 2021, 12, 151 8 of 22 Head and antenna (Figure 6A,B and Figure 7). Head pale testaceous (Figure 6A), slightly narrowed bilaterally; endocarina present, endocarinal line short, one-third as long as frons; frontal sutures distinct along entire length up to antennae; single pair of stem- Head and antenna (Figures6A,B and7). Head pale testaceous (Figure6A), slightly narrowedmata (st) bilaterally; in the form endocarina of prominent present, endocarinal dark pigmented line short, spots one-third with as a long convex as frons; cornea, placed frontalanterolaterally sutures distinct (Figure along 6B). entire Hypopharyngeal length up to antennae; bracon single without pair of median stemmata sclerome. (st) in Setae of thehead form of ofvarious prominent length, dark very pigmented long to spots minute. with aCranial convex cornea,setae: des placed1 elongated, anterolaterally placed medially, (Figure6B). Hypopharyngeal bracon without median sclerome. Setae of head of various des2 elongated, placed posterolaterally, des3 elongated, placed above frontal suture, des4 length, very long to minute. Cranial setae: des1 elongated, placed medially, des2 elongated, slightly shorter than other des, placed anteromedially, des5 elongated placed anterolater- placed posterolaterally, des3 elongated, placed above frontal suture, des4 slightly shorter ally, fs1 as long as des4, placed posteriorly, fs2 short, placed medially, fs3 elongated, placed than other des, placed anteromedially, des5 elongated placed anterolaterally, fs1 as long as desanteromedially,4, placed posteriorly, fs4 andfs2 short,fs5 elongated, placed medially, placedfs 3anterolaterally,elongated, placed close anteromedially, to epistome,fs4 les1 and les2 andas longfs5 elongated, as des4, placedtwo ves anterolaterally, short, postepicranial close to epistome, area withles1 and fourles2 minas long pes as. Antennaedes4, two (Figure 7) veswithshort, oblique postepicranial position area on each with fourside min at anteriorpes. Antennae margin (Figure of head;7) with membranous oblique position basal segment onconvex, each side semi at anterior-spherical, margin bearing of head; conical, membranous moderately basal segment elongated convex, sensorium semi-spherical, and seven sen- bearing conical, moderately elongated sensorium and seven sensilla: Three basiconica (sb), silla: Three basiconica (sb), three styloconica (ss), and one ampullaceum (sa). three styloconica (ss), and one ampullaceum (sa).

FigureFigure 6. 6.Euryommatus Euryommatus mariae mariaemature mature larva, larva, head, frontalhead, view.frontal (A )view. Frontal (A view,) Frontal photo; view, (B) frontal photo; (B) frontal view,view, scheme scheme (at—antenna, (at—antenna, st—stemmata, st—stemmata, setae: des setae:—dorsal des epicranial,—dorsal fsepicranial,—frontal, ls —lateralfs—frontal, epicra- ls—lateral nial, pes—postepicranial). epicranial, pes—postepicranial).

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FigureFigure 7.7. EuryommatusEuryommatus mariaemariaemature mature larva, larva, antenna antenna (SEM (SEM micrograph) micrograph) (sa—sensillum (sa—sensillum ampullaceum, ampul- Se—sensorium,laceum, Se—sensorium, ss—sensillum ss—sensillum styloconicum, styloconicum, sb—sensillum sb—sensillum basiconicum). basiconicum).

MouthMouth partsparts(Figures (Figure8 8A,B,A,B,9 ,Figure 10A–D 9 and, Figure 11A,B). 10A Clypeus–D, and(Figure Figure8 11A,B).A,B) approximately Clypeus (Fig- 3ure× wider8A,B) thanapproximately long, cls1–2 3elongated, × wider than with long, sensillum cls1–2 elongated, (clss) between with them, sensillum all placed (clss) pos- be- terolaterally.tween them, Anteriorall placed margin posterolaterally. of clypeus Anterior straight. Labrummargin of (Figure clypeus8A,B) straight. approximately Labrum (Fig- 2 × widerure 8A,B) than approximately long, anterior margin2× wider almost than long, semicircular; anterior lrsmargin1 medium, almost placed semicircular; anteromedially, lrs1 me- lrsdium,2 elongated, placed anteromedially, placed medially lrs and2 elongatedlrs3 elongated,, placed placed medially posterolaterally. and lrs3 elongated, Epipharynx placed (Figureposterolaterally.8A,B) with Epipharynx three digitate (Figureals, of 8A,B) various with length, three three digitate finger-like als, of variousams: ams length,1 elongated, three amsfinger2 thin,-likeams ams3:short ams1 elongated, and curved; amsmes2 thin,1–2 equal ams3 inshort size, and robust. curved; Labral mes rods1–2 equal (lr) elongated,in size, ro- morebust. sclerotizedLabral rods at(lr) apex elon andgated, wider more towards sclerotized base, at only apex slightly and wider converging towards posteriorly. base, only Sensillaeslightly converging pores (snp) posteriorly. arranged in Sensillae the middle pores of epipharynx:(snp) arranged Two in pairsthe middle close to ofmes epiphar-, next twoynx: pairs Two inpairs the middleclose to of mes labral, next rods. two Surface pairs in of the epipharynx middle of between labral rods. labral Surface rods covered of epi- withpharynx thorn-like between asperities. labral rods Mandibles covered (Figure with thorn9) with-like two asperities. apical teeth Mandibles of unequal (Figure height, 9) with the innertwo apical one subapical teeth of andunequal much height, smaller. the Cutting inner edgeone betweensubapical apex and and much middle smaller. of mandible Cutting with additional protuberance. Setae: mds min, mds medium, both placed laterally in edge between apex and middle of mandible1 with additional2 protuberance. Setae: mds1 shallow pits. Maxillolabial complex (Figure 10A–D) on stipes with one elongated stps, two min, mds2 medium, both placed laterally in shallow pits. Maxillolabial complex (Figure elongated10A–D) onpfs stipes, and with one one min elongatedmbs plus sensillum.stps, two elongated Mala with pfs row, and of one seven min digitate, mbs plus almost sensil- equally-sizedlum. Mala withdms row, and of five sevenvms digitate,(two medium almost and equally three-sized short). dms Maxillary, and five palpi vms with(two twome- palpomeres;dium and three basal short). palpomere Maxillary slightly palpi wider with thantwo distalpalpomeres; one. Length basal palpomere ratio of basal slightly and distal palpomeres almost 1:1. Basal palpomere with one short mps and two pores, distal wider than distal one. Length ratio of basal and distal palpomeres almost 1:1. Basal palpo- palpomere (Figure 11A,B) with one pore, one digitiform sensillum (ds), and a group of mere with one short mps and two pores, distal palpomere (Figure 11A,B) with one pore, 11 apical sensillae (ampullaceae) on terminal receptive area (tra). Dorsal parts of mala one digitiform sensillum (ds), and a group of 11 apical sensillae (ampullaceae) on terminal partially covered with fine asperities. Labium with prementum cup-shaped, with one receptive area (tra). Dorsal parts of mala partially covered with fine asperities. Labium medium prms placed medially. Ligula concave, semicircular at margin, with two min ligs. with prementum cup-shaped, with one medium prms placed medially. Ligula concave, Premental sclerite trident-shaped (median branch weakly sclerotized), posterior extension semicircular at margin, with two min ligs. Premental sclerite trident-shaped (median with elongated, sharp apex; postmentum rather narrow, membranous, triangular, with branch weakly sclerotized), posterior extension with elongated, sharp apex; postmentum three elongated pms: pms1 situated posterolaterally, pms2 mediolaterally and pms3 antero- rather narrow, membranous, triangular, with three elongated pms: pms1 situated posterol- laterally. Labial palpi two-segmented; basal palpomere wider and longer than distal one. aterally, pms2 mediolaterally and pms3 anterolaterally. Labial palpi two-segmented; basal Length ratio of basal and distal palpomeres almost 1:0.7. Each palpomere with single pore, palpomere wider and longer than distal one. Length ratio of basal and distal palpomeres distal palpomere with a group of nine apical sensillae (ampullaceae) on terminal receptive area.almost Lateral 1:0.7. andEach posterolateral palpomere with parts single of labium pore, covereddistal palpomere with prominent with a group asperities. of nine ap- ical sensillae (ampullaceae) on terminal receptive area. Lateral and posterolateral parts of labium covered with prominent asperities.

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FigureFigureFigure 8. 8. 8.Euryommatus Euryommatus mariae mariae mariae mature maturemature larva, larva, larva, clypeus, clypeus, clypeus, labrum labrum labrum,, and, and epipharynx. andepipharynx. epipharynx. (A ()A C) lypeus,Clypeus, (A) Clypeus, la- la- brumlabrum,brum, and, and and epipharynx, epipharynx, epipharynx, photo; photo; photo; (B ()B (cB)lypeus, )clypeus, clypeus, labrum labrum labrum,, and, and and epipharynx, epipharynx, epipharynx, scheme scheme scheme (clss (clss (clss—clypeal——clypealclypeal senso- senso- sen- rium,sorium,rium, ds ds— ds—digitiform—digitiformdigitiform sensillum, sensillum, sensillum, lr —lr—labral lr—labrallabral rods, rods, rods, snp snp— snp—sensillae—sensillaesensillae pore, pore, pore,setae: setae: setae:als als——anterolateral,alsanterolateral,—anterolateral, amsamsams——anteromedial,—anteromedial,anteromedial, clscls cls——clypeal,—clypeal,clypeal, lrslrs lrs——labral,—labral,labral, mmes esm——median).es—median).median).

Figure 9. Euryommatus mariae mature larva, right mandible (mds—mandibular seta). FigureFigure 9. 9.Euryommatus Euryommatus mariae mariae mature mature larva, larva, right right mandible mandible (mds (mds——mandibularmandibular seta). seta).

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Figure 10. Euryommatus mariae mature larva, maxillolabial complex. (A) Maxillolabial complex, ventral view, photo; Figure 10.(B) Euryommatus maxillolabial complex, mariae mature ventral view,larva, scheme; maxillolabial (C) apical complex. part of right (A) maxilla,Maxillolabial dorsal view;complex, (D) apicalventral part view, of right photo; (B) maxillolabialmaxilla, complex, ventral view,ventral (dms view,—dorsal scheme; malar, (Cligs) apical—ligular, partmbs of—malar right maxilla, basiventral, dorsalmps —maxillaryview; (D) apical palp, pfspart—palpiferal, of right maxilla, ventral view,prms—prelabial, (dms—dorsalpms—postlabial, malar, ligsstps—ligular,—stipal, mbsvms—ventral—malar malar).basiventral, mps—maxillary palp, pfs—palpiferal, prms—pre- labial, pms—postlabial, stps—stipal, vms—ventral malar).

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FigureFigure 11.11.Euryommatus Euryommatus mariae mariaemature mature larva, larva, maxillolabial maxillolabial complex complex (SEM (SEM micrographs). micrographs). (A) Maxillo- (A) Maxil- labiallolabial complex, complex, ventral ventral aspect, aspect, SEM SEM photo; photo; (B) apical (B) apical part of part right of maxilla,right maxilla, lateral aspect,lateral SEMaspect, photo SEM (ds—digitiformphoto (ds—digitiform sensillum, sensillum,mps—maxillary mps—maxillary palp seta, palp sa—sensillum seta, sa—sensillum ampullaceum, ampullaceum, sb—sensillum sb—sen- basiconicum,sillum basiconicum, tra—terminal tra—terminal receptive receptive area). area).

3.2. Description of the Pupa of Euryommatus Mariae 3.2. Description of the pupa of Euryommatus mariae Female: BL: 4.00; 4.00; BW: 2.10; 2.50; HW: 0.75; 0.85; RL: 0.80; 0.80; PW: 1.15; 1.25 Female: BL: 4.00; 4.00; BW: 2.10; 2.50; HW: 0.75; 0.85; RL: 0.80; 0.80; PW: 1.15; 1.25 (all (all in mm). in mm). General habitus and chaetotaxy (Figure 12A–F and Figure 13A–C). Body white, slender, cuticleGeneral covered habitus with fineand chaetotaxy asperities, (Figure smooth 12A only– onF and head Figure and pronotum13A–C). Body (Figure white, 12A–F). slender, Rostrumcuticle covered elongated, with 2.8 fine× asasperities, long as wide,smooth reaching only on mesocoxae. head and pronotum Pronotum 1.5(Figure× wider 12A–F). thanRostrum long, elongated, rounded laterally. 2.8× as long Mesonotum as wide, wider reaching than mesocoxae. metanotum. Pronotum Abdominal 1.5 segments× wider than I–IIIlong, of rounded equal length, laterally. segments Mesonotum IV–VI wider tapering than gradually metanotum. towards Abdominal the end segments of the body, I–III of segmentequal length, VII semicircular, segments IV segment–VI tapering VIII narrow, gradually segment towards IX terminal,the end of with the urogomphibody, segment (ur)VII semicircular, medially situated, segment slightly VIII recurved, narrow, segment elongated, IX coveredterminal, with with asperities, urogomphi each (ur) with medi- sclerotized,ally situated, anchor–like slightly recurved, apex. Spiracles elongated, placed covered dorso-laterally with asperities, on abdominal each segments with sclerotized, I–VI, functionalanchor–like on apex. segments Spiracles I–V, vestigial placed dorso on segment-laterally VI. on Chaetotaxy abdominal (setal segments numbers I–VI, are functional given foron onesegments side of I the–V, body):vestigial Setae on variable segment in VI. size, Chaetotaxy hair-like on (setal head andnumbers rostrum, are thorn-likegiven for one onside thorax of the and body): abdomen, Setae all variable placed on in prominentsize, hair-like protuberances. on head and Head rostrum, with two thornpas-likeof on variousthorax and sizes abdomen, and three os allof placed unequal on length, prominent rostrum protuberances. with one rs (Figure Head 13 withA–C). two Pronotum pas of vari- with one as, one ls, one sls, one ds, and three pls almost equal in size. Meso- and metathorax ous sizes and three os of unequal length, rostrum with one rs (Figure 13A–C). Pronotum with two short setae placed medially on dorsum. Abdominal segments I–VI with three with one as, one ls, one sls, one ds, and three pls almost equal in size. Meso- and metathorax short setae (d placed medially, d , and d more laterally). Segment VII with three (segment with two short1 setae placed medially2 3 on dorsum. Abdominal segments I–VI with three VIII with 2) thorn-like, robust setae, placed on elongated protuberances. Each side of segmentshort setae IX ( withd1 placed single medially, robust, thorn-liked2, and d3 more seta placed laterally dorsolaterally,). Segment VII and with urogomphus three (segment placedVIII with dorsomedially. 2) thorn-like, Lateral robust andsetae, ventral placed parts on elongated of abdominal protuberances. segments I–VIII Each without side of seg- setae.ment EachIX with femur single with robust, two elongated, thorn-like hair-like seta placed setae dorsolaterally (Figure 13A–C)., and urogomphus placed dorsomedially. Lateral and ventral parts of abdominal segments I–VIII without setae. Each femur with two elongated, hair-like setae (Figure 13A–C).

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FigureFigure 12. 12. EuryommatusEuryommatus mariae mariae pupapupa (SEM (SEM micrographs). micrographs). (A) (HAabitus,) Habitus, ventral ventral view; view; (B) head, (B) head, frontalfrontal view, view, apical apical part; part; (C (C) rostrum) rostrum base, base, lateral lateral view; view; (D) ( Dabdomen,) abdomen, ventral ventral view, view, magnification; magnifica- (tion;E) gonothecae; (E) gonothecae; (F) urogomphus (F) urogomphus (ur— (ur—urogomphus,urogomphus, setae: setae: d—dorsal,d—dorsal, fes—femoral,fes—femoral, os—orbital,os—orbital, rs— rostral).rs—rostral).

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Figure 13. 13. EuryommatusEuryommatus mariae mariae pupa,pupa, habitus habitus,, and chaetotaxy. and chaetotaxy. (A) Ventral (A) Ventralview; (B view;) dorsal (B view;) dorsal view; (C) lateral view (Th. I–III—pro-, meso-, and metathorax, Abd. I–IX—abdominal segments 1–9, (C) lateral view (Th. I–III—pro-, meso-, and metathorax, Abd. I–IX—abdominal segments 1–9, ur—urogomphus, setae: as—apical, d—dorsal, ds—discal, fes—femoral, ls—lateral, os—orbital, ur—urogomphus,pas—postantennal, pls setae:—posterolateral,as—apical, d rs—dorsal,—rostral,ds sls—discal,—super lateral).fes—femoral, ls—lateral, os—orbital, pas— postantennal, pls—posterolateral, rs—rostral, sls—super lateral). 3.3. Description of the Adults of Euryommatus Mariae 3.3. Description of the Adults of Euryommatus Mariae In Europe, Euryommatus mariae is the only member of its genus and a morphologi- cally Indistinct Europe, species,Euryommatus included mariaein severalis the identification only member keys of its[28 genus–30]. This and small a morphologically weevil distinct(body length species, 3.3–4.2 included mm in studied in several specimens) identification is easily keys and [immediately28–30]. This distinguishable small weevil (body length 3.3–4.2 mm in studied specimens) is easily and immediately distinguishable from all other European weevils by its habitus (Figure 14A): The abdominal ventrites rising steeply posterad and covered with flattened elytra, weakly sloping apicad (Figure 14B); the hypognathous head with enlarged eyes covering its entire dorsum and separated just by a Insects 2021, 12, 151 15 of 22

thin integumental septum no thicker than twice the diameter of a minute ommatidium; the prosternum lacking any trace of a rostral canal; the large and prominent mesepimera; the broad metanepisterna; the round scutellar shield surrounded by a deeply impressed ring; the posterior margins of abdominal ventrites 2–4 expanded vertically, bare and shiny Insects 2021, 12, x FOR PEER REVIEW(Figure 14C); the large, sharp tooth on the fore femur and the vestigial17 teeth of 24 on the mid-

and hind femora, and all the tibiae shorter than the femora.

FigureFigure 14. 14. EuryommatusEuryommatus mariae mariae adult.adult. (A, D–I (D;A E; F;,D G; H;– I;I) )M Male;ale; (B, (CB) ,female;C) female; (A) habitus, (A) habitus, dorsal view dorsal view (body (body length 3.7 mm); (B) habitus, lateral view (body length 4.2 mm); (C) margins of abdominal lengthventrites 3.7 2– mm);4 posterior (B) habitus,view; (D) lateralconnate view hemisternites (body length VIII; (E) 4.2 tergite mm); VII; (C (F)) marginspygidium, of dorsal abdominal ventrites 2–4view; posterior (G) same, view; dorso- (posteriorD) connate view; hemisternites (H) aedeagus in VIII;lateral ( Eview,) tergite showing VII; full (F )ejaculatory pygidium, duct dorsal view; (G) same,(broken dorso-posterior in a few places— view;the specimen (H) aedeagus was processed in lateral several view, times) showing protected full by ejaculatorya fibrous con- duct (broken in a duit (x—fibrous structure of the conduit seen under high magnification under the compound mi- few places—the specimen was processed several times) protected by a fibrous conduit (x—fibrous croscope; y—portion of true membranous ejaculatory duct visible after disconnection of the con- structureduit); (I) aedeagus of the conduit in dorsal seen view, under showing high the magnification tegmen, orificial under sclerites the, and compound endophallic microscope; spinose y—portion ofbrush. true membranous ejaculatory duct visible after disconnection of the conduit); (I) aedeagus in dorsal view, showing the tegmen, orificial sclerites, and endophallic spinose brush. Female. Abdominal ventrite 5 only with appressed scales. Tergite VII trapeziform, only The1.5–1.6 male × as andbroad female as long, terminalia broadly rounded of E. apicmariaeally,have in its entirety never beenheavily described sclerotized or illustrated, and coarsely punctate, with wing-folding patches smaller than in male, with a complete albeittransverse Wanat carina [31 separating] did mention apical part the unusuallywith much smaller long ejaculatoryand sparser punctures duct, supplying bearing a photo of aedeaguslonger setae in (Figure support 15A of). Tergite his statement. VIII sub-pentagonal Examination in shape, of the markedly postabdomen tapering from revealed several charactersbasal third whichto apex, may wholly serve concealed to distinguish beneath tergite this species VII in repose, from its weakly congeners. and evenly One of them, the structuresclerotized of except the endophallus for a narrow, clear and especiallymedian line ofin proximal the ejaculatory two-thirds; duct, apical is unusual one-third and probably unknowndensely setose, in other with setae weevils. progressively The structure longer towards of the postabdomen tergum apex (Figure is described 15B). Spicu- and illustrated belowlum ventrale for diagnostic (Figure 15C) purposes. with short apodeme; sternal plate large, with a median sclero- tized fork and largely desclerotized margins, bearing about a dozen long setae on apices Male abdominal ventrite 5 apically with a paired tuft of protruding setae. Tergite VII of fork arms. Ovipositor consisting of subrectangular coxites about twice as long as broad stronglyand tightly transverse, joined to the ca folded 2.2–2.3 membrane× as broad (Figure as 15D) long and in thestylimiddle, attached withlatero- shortapically anterior arms, apicallyto coxites, shallowly large, strongly emarginate, elongate, not in itsless entirety than 0.4 heavily× as long sclerotizedas coxite, numerous and coarsely long punctate, with large lateral wing-folding patches (Figure 14E). Pygidium (tergite VIII) exposed from

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elytra in repose, apically with a large impression bordered by sharp carinae, an impres- sion in the middle with paired, small, lighter windows, on sides with dense raised scales (Figure 14F,G). Hemisternites VIII, large and broadly connate medially (Figure 14D). Spicu- lum relictum on membrane fold between sternites VIII and IX absent, even as a membra- nous process. Tegmen with apodeme much shorter than forked basal piece; parameral lobes long and narrow, ca 2/3 as long as pedon, each with median sclerotized stripe. Pedon in profile sharply hooked apically (Figure 14H); ostium with large paired sclerites (Figure 14I). Membranous endophallus small and fully contained in pedon. The whole ejaculatory duct in a peculiar, sclerotized conduit-like sheath composed of dense fibrae and unstainable with Chlorazol black (Figure 14H), a few times longer than the ’s body itself (!), in repose looped many times outside the penis proper, tightly folded into a package adjoining ventral side of pedon and its apodemes; the rigid sheath enters the pedon through the basal foramen and near the orifice joins an elongate brush of large and partly radiate spines. Female. Abdominal ventrite 5 only with appressed scales. Tergite VII trapeziform, only 1.5–1.6 × as broad as long, broadly rounded apically, in its entirety heavily sclerotized and coarsely punctate, with wing-folding patches smaller than in male, with a complete transverse carina separating apical part with much smaller and sparser punctures bearing longer setae (Figure 15A). Tergite VIII sub-pentagonal in shape, markedly tapering from basal third to apex, wholly concealed beneath tergite VII in repose, weakly and evenly sclerotized except for a narrow, clear median line in proximal two-thirds; apical one- third densely setose, with setae progressively longer towards tergum apex (Figure 15B). Spiculum ventrale (Figure 15C) with short apodeme; sternal plate large, with a median sclerotized fork and largely desclerotized margins, bearing about a dozen long setae on apices of fork arms. Ovipositor consisting of subrectangular coxites about twice as long as Insects 2021, 12, x FOR PEER REVIEW 18 of 24 broad and tightly joined to the folded membrane (Figure 15D) and styli attached latero- apically to coxites, large, strongly elongate, not less than 0.4 × as long as coxite, numerous long setae along entire apex, i.e., 0.4 × length of stylus. Vagina composed of simple, butseta thicke along and entire multi-folded apex, i.e., 0.4 membrane. × length of Bursastylus. narrow,Vagina composed unilobed, of composed simple, but of thick simple fine membrane.and multi-folded Spermatheca membrane. small, Bursa C-shaped, narrow, withunilobed, spherical composed corpus of lacking simple fine prominences mem- and brane. Spermatheca small, C-shaped, with spherical corpus lacking prominences and nar- narrower cornu (Figure 15E); gland relatively large, elongate; spermathecal duct very long, rower cornu (Figure 15E); gland relatively large, elongate; spermathecal duct very long, unsclerotized, in its entirety tightly spiral (Figure 15D,E). unsclerotized, in its entirety tightly spiral (Figures 15D,E).

FigureFigure 15. EuryommatusEuryommatus mariae mariae adultadult female. female. (A) T (ergiteA) Tergite VII; (B VII;) tergite (B) tergiteVIII; (C VIII;) spiculum (C) spiculum ventrale; ventrale; (D(D)) ovipositor,ovipositor, vagina, vagina, bursa bursa copulatrix copulatrix,, and andmajor major portion portion of spermathecal of spermathecal duct; (E) duct; spermatheca (E) spermatheca with its gland and adjoining portion of the broken spermathecal duct. with its gland and adjoining portion of the broken spermathecal duct. 4. Discussion The host associations and basic details of larval development have been identified in just one European species from each genus within the tribe Coryssomerini. Coryssomerus capucinus lives on several herbaceous from the genera Tripleurospermum Sch. Bip., Achillea L., Chrysanthemum L., and Anthemis L. (Asteraceae); its larva develops in the root neck and pupates in the soil [32,33]. The biology of Euryommatus mariae is quite different, however: It has saproxylic, subcortical larvae associated with gymnosperm trees. Such an association between conifers and saproxylic larvae is unknown in any other Palaearctic member of the supertribe Conoderitae. However, analogous host associations with conif- erous trees and wood-boring larvae have been well documented in several Nearctic spe- cies of the genus Cylindrocopturus, classified in the tribe [34], and distributed along Pacific coast of North America [35]. According to Furniss and Carolin [36], they attack the twigs and boles of various conifers, including pine (Pinus L.), true fir (Abies L.), Douglas fir (Pseudotsuga Carrière), larch (Larix Mill.), and hemlock (Tsuga Carrière). The Douglas fir twig weevil Cylindrocopturus furnissi Buchanan develops on Pseudotsuga men- ziesii (Mirbel) Franco [37], while C. eatoni Buchanan, known as the pine wee- vil, attacks primarily ponderosa and Jeffrey pines (Pinus ponderosa Douglas ex C.Lawson, P. jeffreyi Balf.). Although associated with conifers in much the same way as E. mariae, the biology of these Nearctic Cylindrocopturus species is significantly different. They both at- tack the branches and boles of saplings and young trees with green foliage and develop in living wood, their larvae often killing them by destroying the phloem and cambium, thus cutting off sap transport. The larvae of C. eatoni can be found in all woody parts of pine saplings, even in the rootstock some centimetres below ground level, but the top of

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4. Discussion The host associations and basic details of larval development have been identified in just one European species from each genus within the tribe Coryssomerini. Coryssomerus capucinus lives on several herbaceous plants from the genera Tripleurospermum Sch. Bip., Achillea L., Chrysanthemum L., and Anthemis L. (Asteraceae); its larva develops in the root neck and pupates in the soil [32,33]. The biology of Euryommatus mariae is quite different, however: It has saproxylic, subcortical larvae associated with gymnosperm trees. Such an association between conifers and saproxylic larvae is unknown in any other Palaearctic member of the supertribe Conoderitae. However, analogous host associations with conifer- ous trees and wood-boring larvae have been well documented in several Nearctic species of the genus Cylindrocopturus, classified in the tribe Zygopini [34], and distributed along Pacific coast of North America [35]. According to Furniss and Carolin [36], they attack the twigs and boles of various conifers, including pine (Pinus L.), true fir (Abies L.), Douglas fir (Pseudotsuga Carrière), larch (Larix Mill.), and hemlock (Tsuga Carrière). The Douglas fir twig weevil Cylindrocopturus furnissi Buchanan develops on Pseudotsuga menziesii (Mirbel) Franco [37], while C. eatoni Buchanan, known as the pine reproduction weevil, attacks primarily ponderosa and Jeffrey pines (Pinus ponderosa Douglas ex C.Lawson, P. jeffreyi Balf.). Although associated with conifers in much the same way as E. mariae, the biology of these Nearctic Cylindrocopturus species is significantly different. They both attack the branches and boles of saplings and young trees with green foliage and develop in liv- ing wood, their larvae often killing them by destroying the phloem and cambium, thus cutting off sap transport. The larvae of C. eatoni can be found in all woody parts of pine saplings, even in the rootstock some centimetres below ground level, but the top of the stem and the upper branches are infested much more abundantly [38]. C. furnissi also attacks small living trees of Douglas fir, and in older ones it evidently prefers the previous four years’ growth for oviposition, frequently killing scattered small branches [36]. In both Cylindrocopturus species, the eggs are laid individually in holes chewed by the female in living bark—globules of resin produced by the tree reveal their locations. Their larvae bore galleries in cortical tissue, phloem or even pith, and often pupate there in thin twigs, while in thicker branches and the trunk, mature larvae usually work their way into the outer layer of wood for pupation. The different habits of Euryommatus mariae can be inferred from the data collected at the Cisów site. There, the weevil seems to be confined to dead or dying spruce branches, presumably weakened and dying lower laterals, subsequently appearing on older trees that retain their bark intact for quite a long time after death. Unlike the American conifer beetles Cylindrocopturus, E. mariae is a saproxylic species utilizing the outermost layer of dead or dying wood. Apart from this basic difference in diet, many other aspects of the biology of E. mariae appear to resemble that of the above-mentioned Cylindrocopturus species. Their development takes a year with a winter break [36–38], an aspect that also appears to hold true for E. mariae, where the larva is the diapausing stage. In its phenology, too, E. mariae seems to follow C. furnissi in particular. This latter species starts to make feeding holes in the bark of small Douglas fir branches, mating, and laying eggs after mid-June, with adults leaving the pupal chambers by the beginning of August [37]. The emergence of the adults of C. eatoni begins about a month earlier, already in late May, and peaks in mid- June, when the weevils can be found feeding abundantly on pine needles [38]. Although the larvae collected in Cisów on 22 March pupated in the same month, and one adult emerged on 1 March from material preserved early in winter, they were all reared under laboratory conditions at room temperature, which could have speeded up metamorphosis considerably. The numerous adults of E. mariae obtained by Rutkiewicz [12] from the screen-trunk traps deployed in Cisów are all dated to the end of August. Moreover, the recent collections of this species took place in mid-August in Germany [13], and in mid-July in Austria [14]. The morphology of immatures of species from the tribe Coryssomerini remains poorly studied. Only the paper by Urban [39] contains some basic, unillustrated information Insects 2021, 12, 151 18 of 22

about the larva and pupa of Coryssomerus capucinus (Beck, 1817), subsequently published by Scherf [32]. Urban [39] highlighted the larval cuticle densely covered with hook-like asperities, six variously long setae on each of the pedal lobes, the two-segmented labial palpi, and bifid mandibles. Unfortunately, other characters are either very common or were described inaccurately. But it is noteworthy that the larval cuticle of Euryommatus mariae exhibits a very similar structure to that of the larva of C. capucinus. Urban’s [39] description of the pupa of C. capucinus did not contribute any significant information. Hinz and Müller-Schärer [40] reported five larval instars of C. capucinus based on the width of the head capsule. According to these authors, the head width of the premature larva is 0.70 mm, while in the mature larva it is 0.93 mm [40]. Both values resemble the head measurements of E. mariae (0.70 mm and 0.95 mm). From this, one may presume that the larval development of E. mariae also involves five instars. Despite the highly precise measurements, the paper by Hinz and Müller-Schärer [40] does not contain any other information about the larval morphology. Thus, the descriptions of the larva and pupa of E. mariae given here are the first complete, illustrated information on immatures of the tribe Coryssomerini. It seems that the immatures of most genera belonging to the subfamily Conoderinae Schoenherr have yet to be described. The only exceptions are a few species from the tribe Zygopini (regarded as pests of silviculture): The genus Cylindrocopturus—C. crassus van Dyke, Keifer [41], C. quercus (Say) [42], and C. furnissi Buchanan [43], and a single species from the genus Eulechriopus—E. gossypii Barber Böving [44]. Analysis of these papers is sometimes difficult, however, because of the different nomenclature used in them and the lack of descriptions of certain structures: For instance, the abdominal setae of E. gossypii, according to Böving [44] are extremely small and impossible to count accurately. Compared with the larvae of other Conoderinae species, the larva of E. mariae reveals some important, original features, different from Cylindrocopturus, and in some cases, Eulechriopus, such as: (1) Single as (vs. two as); Abd. VIII with three pds (vs. two ds); Abd. IX with three ds and three ps (vs. two ds and two ps); (3) head rounded (vs. narrowed bilaterally); (4) abdominal segments dorsally with transverse rows of elongate plate-like asperities, each parallel to long body axis and with anterior and posterior denticle (vs. only the simple, thorn-like asperities); (5) erect setae on thorax and abdominal segments VIII and IX very long, evidently longer than on the remaining abdominal segments (vs. setae on all body segments subequally short). The best visible common characters of the genera Cylindrocopturus and Euryommatus include the extended head; the single pair of ocelli placed close to the antenna; the frons with five setae; the mala with seven dms, and five vms; the clypeus with very long setae; the structure of the spiracles; the dorsal folds of the abdominal segments I–VII divided into three lobes; the well-developed abdominal setae; the prothorax with 10 (11 on C. furnissi) prms; each pedal lobe with six pda; the meso- and metathorax each with one prs and four pds; each of abdominal segments I–VII with one prs, five (four on C. quercus) pds, two ss, two eps, and two ps. On the other hand, the larva of E. gossypii displays many original characters, different from both Cylindrocopturus and Euryommatus, above all the strongly retracted head and the structure of the last abdominal segments closely resembling the type “B” described by van Emden [45], found, for example, on Tanymecus, Strophosoma and Philopedon [46]. Moreover, the larva of Eulechriopus has the dorsal folds of abdominal segments I–VII divided into two lobes, two pairs of ocelli, and the clypeus without setae [44]. The larval characters common to all Conoderinae genera are (1) endocarina present; (2) conical, moderately elongated antennal sensorium; (3) epipharynx with three als, three ams, and two mes; (4) labral rods very elongated, slightly converging posteriorly; (5) bifid mandible; (6) two-segmented labial palpi; (7) dorsal part of the body densely covered with asperities; (8) all spiracles bicameral. Based on head width measurements of C. quercus, Piper [42] reported three larval instars: The first 0.18–0.19 mm, the second 0.23–0.24 mm, and the third 0.50–0.72. Hence, Insects 2021, 12, 151 19 of 22

GF takes a value of 1.35 between the first and second instars (1.32 on C. capucinus), but 2.60 between the second and third instars (1.41 on C. capuccinus). Moreover, GF measured between the smallest and largest larvae, assessed by Piper [42] as third instars, takes a value of 1.44, which is similar to the GF estimated between the fourth and fifth instars of C. capucinus [40]. Hence, the measurements performed with the GF proposed by Dyar [47] indicates (most probably) the existence of five larval instars in C. quercus. According to Böving [44], the pupae of E. gossypii and C. crassus are visibly similar in shape; this may also apply to the pupae of C. furnissi [43], C. quercus [42], and in some ways to E. mariae, mainly because of the great morphological similarity of the adult stages of those species. However, the lack of accurate drawings and precise nomenclature of the chaetotaxy does not permit any far-reaching inferences to be drawn. Anderson [43] described the urogomphi of C. furnissi as being placed laterally, “slightly sclerotized at the tip and terminating in two or three minute projections”. It is hard to say whether the structure described by Anderson [43] is something that corresponds to the urogomphi of E. mariae. The pupa of E. mariae has quite elongated urogomphi with anchor-like apices, placed dorsomedially, which is rather uncommon in weevil pupae and well visible. Thus, it does not seem possible that such a crucial feature has been overlooked in the descriptions of Cylindrocopturus and Eulechriopus. Ultimately, however, it is impossible to distinguish any features of taxonomic importance for Conoderitae, based on existing descriptions of these pupae. The study of the adult postabdomen has yielded several morphologically and evo- lutionarily noteworthy discoveries. The unusually long ejaculatory duct protected by a fibrous sheath is a unique character of E. mariae, not found in its congeners available for this study, or in Coryssomerus from the same tribe. However, an unidentified Euryommatus sp. from Fethiye in southern Turkey (coll. M. Wanat) possesses in its endophallus a flagellum- like pipe of similar fibrous structure, though incomparably shorter, not exceeding the tips of the penile apodemes. On the other hand, the ejaculatory duct in another Euryommatus sp. from the Myohyang Mts. in North Korea (coll. Museum and Institute of Zoology, Polish Academy of Sciences, Warsaw) is completely different, broad and tape-like, and unprotected by any additional sheath. The functionalism of such a bizarre ejaculatory duct and the mechanics of copulation in E. mariae remain unknown and are difficult to imagine. The only observed peculiarity in the structure of the female postabdomen, eventually in response to the male modification, is the extraordinarily long and spiral spermathecal duct. This might suggest the penetration and spreading of this duct by the peculiar rigid male conduit. This hypothesis is supported by the fact that, as shown in (Figure 15D), the spermathecal duct thickens progressively towards the bursa and is visibly broader near its opening than at its spermathecal end. If confirmed by direct observation, possibly based on the immediate freezing of mating individuals, this would be a striking example of evolutionary competition between sexes.

5. Conclusions The larvae and pupae of Euryommatus mariae (Coryssomerini) were reared from dead spruce Picea abies branches collected in central Poland. Its association with coniferous trees from the family Pinaceae, highlighted in the literature, is thus confirmed, even though spruce has never actually been mentioned as a potential host of this weevil. The species turned out to be saproxylic, in contrast to several Nearctic species of Cylindrocopturus (Zygopini) that develop in the living tissues of various American conifers and have a similar life cycle and phenology. The very limited knowledge of the morphology of the immature stages of Conoderitae hinders comparisons and estimates of differences. The larva of E. mariae shares the cuticle densely covered by thorn-like asperities with both Coryssomerus and the members of Cylindrocopturus, and probably also with Eulechriopus (both Zygopini), although in the last-mentioned genus, the description of this character in E. gossypii in Böving [44] was inaccurate. This peculiar character, thus, appears to be common to a wider group of genera Insects 2021, 12, 151 20 of 22

of Conoderitae. The unique larval characters of E. mariae, not recorded in the other genera being compared here, are the single alar seta (as) (vs. two as), the abdominal segment VIII (Abd. VIII) with three postdorsal setae (pds) (vs. two dorsal setae (ds)), and the rounded head (vs. narrowed bilaterally), and elongate, bicornuate plate-like asperities arranged in transverse rows on the dorsum of abdominal segments, the character not known in other weevil larvae. The most easily observed diagnostic character of E. mariae is the presence of numerous long, erect setae on thoracic segments I–III and abdominal segments VIII–IX. These were not reported in any of the species compared, in which all the dorsal setae are short to poorly discernible. This may be a consequence of saproxylic mode of larval life of E. mariae, in the galleries bored under loose bark of dead tree branch, where the larva has to control more space than the larvae of other compared species boring a narrow channel in tight living tissues. Euryommatus mariae is widely distributed in the taiga zone of Eastern Palaearctic [3–7], whilst in Europe it seems to be very local and relict species found in just a few spots of natural coniferous forests in both the mountains (the type locality, Austria, Germany), and the lowlands (Latvia, Poland). Its disjunct distribution summarized in Figure 16, the apparent confinement to large and natural or semi-natural forests of boreal type, and the Insects 2021, 12, x FOR PEER REVIEWevidenced association with deadwood, all support well the selection of E. mariae22 forof 24 the

group of umbrella species in forest conservation [48]. The species is sporadically collected, and despite a very large area of distribution, the number of documented records is very low,low, eithereither inin EuropeEurope or Asia. It It makes makes uncertain uncertain the the gap gap in in its its range range between between Siberia Siberia and and Europe,Europe, resultingresulting from the hitherto hitherto literature literature records. records.

FigureFigure 16.16. Distribution of of EuryommatusEuryommatus mariae mariae inin Asia Asia (shaded (shaded area) area) and and Europe Europe (dots). (dots). Map Map based based on an image obtained from the Demis World Map Server open source (http://web- on an image obtained from the Demis World Map Server open source (http://webmap.iwmi.org/ map.iwmi.org/DataSrc.htm, currently unavailable). DataSrc.htm, accessed on 22 December 2020, currently unavailable). The unusually long male ejaculatory duct protected with a fibrous sheath is a unique The unusually long male ejaculatory duct protected with a fibrous sheath is a unique character of E. mariae, probably unknown in other weevils (Curculionoidea). This con- character of E. mariae, probably unknown in other weevils (Curculionoidea). This contrasts trasts with the extremely long female spermathecal duct, which, moreover, is spiral along with the extremely long female spermathecal duct, which, moreover, is spiral along its its whole length. These two striking characters seem to be correlated and suggest the pos- whole length. These two striking characters seem to be correlated and suggest the possible sible deep penetration of the spermathecal duct by the male with his half-rigid ejaculatory deep penetration of the spermathecal duct by the male with his half-rigid ejaculatory duct duct sheath; but this will have to be confirmed by direct observation. sheath; but this will have to be confirmed by direct observation. Author Contributions: Conceptualization—R.G. and M.W.; methodology—R.G., M.W. and M.B.; Authorfield research Contributions:—M.B. andConceptualization—R.G. M.W.; laboratory resources and—M.W. M.W.; and methodology—R.G., M.B.; data curation— M.W.R.G. and and M.B.; fieldM.W.; research—M.B. writing—original and draft M.W.; preparation laboratory—R.G. resources—M.W. and M.W.; writing and— M.B.;review data and curation—R.G.editing—R.G. and M.W.;and M.W.; writing—original visualization— draftR.G. preparation—R.G. and M.W. All authors and have M.W.; read writing—review and agreed to the and published editing—R.G. ver- and M.W.;sion of visualization—R.G. the manuscript. and M.W. All authors have read and agreed to the published version of the manuscript. Funding: This research received no external funding. Funding: This research received no external funding. Data Availability Statement: The data presented in this study are available in this article. Data Availability Statement: The data presented in this study are available in this article. Acknowledgments: The authors thank Henry A. Hespenheide for his help with the literature que- ries and his comments on the diversity, biology and morphology of the American Conoderitae, also Paweł Jałoszyński for the photograph of the larval gallery of Euryommatus mariae. Peter Senn is thanked for linguistic corrections. The authors are grateful to four anonymous reviewers for their comments, suggestions and improvements. Conflicts of Interest: The authors declare no conflict of interest.

References 1. Prena: J.; Colonnelli, E.; Hespenheide, H.A. Conoderinae Schoenherr, 1833. In Handbook of Zoology, Coleoptera; Leschen, R.A.B., Beutel, R.G., Eds.; DeGruyter: Berlin, Germany, 2014; Volume 3, pp. 577–589. 2. Anderson, R.S. Meeting of Weevil Workers at 1997 Entomological Society of America Meetings in Nashville. 1998, 43, 8–11. 3. Lyal, C.H.C. Conoderinae. In Catalogus Coleopterorum Palearcticae, Curculionoidea II; Löbl, I., Smetana, A., Eds.; Brill: Leiden, The Netherlands; Boston, MA, USA, 2013; Volume 8, pp. 214–217. 4. Alonso–Zarazaga, M.A.; Barrios, H.; Borovec, R.; Bouchard, P.; Caldara, R.; Colonnelli, E.; Gültekin, L.; Hlaváč, P.; Korotyaev, B.; Lyal, C.H.C.; et al. Cooperative Catalogue of Palaearctic Coleoptera Curculionoidea.Sociedad Entomológica Aragonesa, Monografias Electrónicas SEA, 8. Available online: www.sea–entomologia.org (accessed on 13 November 2020). 5. Kojima, H.; Morimoto, K. An Online Checklist and Database of the Japanese Weevils (Insecta: Curculionidae: Curculionoidea) (excepting Scolytidae and Platypodidae). Bull. Kyushu Univ. Mus. 2004, 2, 33–147.

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Acknowledgments: The authors thank Henry A. Hespenheide for his help with the literature queries and his comments on the diversity, biology and morphology of the American Conoderitae, also Paweł Jałoszy´nskifor the photograph of the larval gallery of Euryommatus mariae. Peter Senn is thanked for linguistic corrections. The authors are grateful to four anonymous reviewers for their comments, suggestions and improvements. Conflicts of Interest: The authors declare no conflict of interest.

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